The Hooded Crow (Corvus cornix) as an EnvironmentalBioindicator Species of Heavy Metal Contamination

Mauro Giammarino • Piero Quatto •

Stefania Squadrone • Maria Cesarina Abete

Received: 9 March 2013 / Accepted: 13 August 2014 / Published online: 23 August 2014

� Springer Science+Business Media New York 2014

Abstract This study aims to examine the possible pre-

sence of lead and cadmium in the liver and kidneys of

hooded crows (Corvus cornix). Liver and kidneys of hoo-

ded crow carcasses were collected in Province of Cuneo

(Piedmont, Italy) in order to detect lead and cadmium

content. Significant differences were found in lead and

cadmium levels between areas of intensive cultivation

versus areas where meadows are prevalent. Moreover, age

greatly influenced the burden of heavy metals, while sex

did not seem to affect the level of contamination. The

source of contamination may be phosphate fertilizers used

for intensive cultivation in the study area.

Keywords Heavy metals � Corvus cornix � Bioindicator

species � Cadmium � Lead

Lead (Pb) and cadmium (Cd) from phosphate fertilizers

pose a potentially serious threat to soil quality and, via the

food chain, to human health (Alloway and Steinnes 1999;

Sheppard et al. 2009). Heavy metals that are present in

fertilizers remain in the ground and are absorbed by

organic components, thus contaminating surface water.

These elements are absorbed by plants (Adams et al. 2004),

especially in acidified soils, and are then consumed by the

animals, including humans. Once absorbed, cadmium and

lead bioaccumulate in high concentrations in liver and

kidneys (Godt et al. 2006). This cycle may cause the

decline of populations of some avian species in intensively

farmed areas (BTO 2012). This may also directly affect

humans that consume contaminated water and plants and

animals, and secondary contamination of lead and cad-

mium in edible parts of animals is also of concern

(Bilandzic et al. 2010).

It is objectively difficult to define the metal levels

related to a state of toxicity or mortality, or to a geo-

chemical background, in the tissues and organs of wild

birds. The majority of reports on this subject are on

waterfowl (Guitart et al. 1994), seabirds and raptors (Kal-

isinska et al. 2006), while there are few studies on passe-

rines. Studies have frequently utilized feathers, feces and

eggs as organic matrices (Dauwe et al. 2000; Mora 2013;

Swaileh and Sansur 2006; Berglund et al. 2011; Markowski

et al. 2013). Nonlethal collection methods can be used to

detect heavy metal levels and constitute a valid technique

to assess environmental contaminants. However, monitor-

ing the concentrations of contaminants within the tissues is

an useful way of assessing the potential damage of chem-

icals to organisms and their predators or scavengers. Liver

and kidneys are the most important organs for detoxifica-

tion processes. The spleen and pancreas are the only pos-

sible alternatives to liver and kidneys in lead poisoning

diagnostic procedures (Guitart et al. 1994).

Lead poisoning manifests itself as a chronic or acute

disease in wild birds. Signs usually include progressive

M. Giammarino (&)

Department of Prevention Asl CN 1, Cuneo, Via San Quirico

53/7, 10042 Nichelino, TO, Italy

e-mail: iammino@libero.it

P. Quatto

Department of Economics, Management and Statistics,

University of Milano-Bicocca, Piazza dell’Ateneo Nuovo,

1, 20126 Milan, Italy

e-mail: piero.quatto@unimib.it

S. Squadrone � M. C. Abete

Istituto Zooprofilattico Sperimentale del Piemonte, Liguria

e Valle d’Aosta, Via Bologna 148, 10154 Turin, Italy

M. C. Abete

e-mail: mariacesarina.abete@izsto.it

123

Bull Environ Contam Toxicol (2014) 93:410–416

DOI 10.1007/s00128-014-1362-y

weakness, green-stained feces and vent, deposition of eggs

with thin shells, disorders of the central nervous system

(Burger 1995), weight loss and emaciation, as well as

making no attempt to escape in the presence of humans.

Lesions consist of severe wasting of breast muscles,

impaction of esophagus or proventriculus, enlarged gall-

bladder containing dark green bile, and hemorrhagic

enteritis. High levels of lead exposure decreases resistance

to infectious disease (Gainer 1974) and can result in nest-

ling and adult death (Clark and Wilson 1981).

Cadmium is an extremely toxic element; it is able to

cause both acute and chronic tissue lesions and has been

found to have teratogenic, mutagenic and carcinogenic

effects (Krajnc et al. 1987).

The aim of this study is to determine the prevalence of

lead and cadmium levels in hooded crows (Corvus cornix)

collected from province of Cuneo (Piedmont, Italy) and to

compare the levels recorded in hooded crows that reside in

intensely cultivated territory where chemical fertilizers are

used, with those of hooded crows that reside in regions

used for pasture where no chemical fertilizers are used.

Cuneo is a province in the southwest of the Piedmont

region of Italy (Fig. 1). The municipalities included in the

monitoring plan are located in the Po valley.

Hooded crows are quite sedentary, never venturing far

from their nests and can therefore be considered as residing

in this contained area. In addition, their propensity to

scavenge, their trophic level, and the fact that they are

abundant, makes them candidates for bioindicators of

environmental contamination by lead and cadmium

(Spellerberg 1991). The crow may be contaminated either

by consuming water and forage directly or by eating animal

carcasses with the pollutants. We have found no data in the

literature regarding the hooded crow, nor any data relating

to other passerines in this study area.

The present paper reports on lead and cadmium pollu-

tion in kidney and liver of hooded crown (C. cornix). The

possible role as bioindicator species of the environmental

contamination of heavy metal is investigated. This species

is considered damaging for the area considered and it is

under a plan of control. Then liver and kidney from of

hooded crown are easily available and constitute useful

specimen to assess the heavy metals contamination of rural

territories. We hypothesize that the habitat of hooded crows

heavily influences the levels of heavy metals in its organs.

In particular the specimens living in highly cultivated areas

where fertilizers are extensively used can adequately reflect

the level of environmental pollution. In addition we want to

verify if C. cornix age or gender can affect the levels of

cadmium and lead in the tissues examined, in order to

identify the parameters that make this species a good

environmental indicator.

Materials and Methods

Hooded crows were caught with Larsen traps placed in five

different localities in the Cuneo plain (district of Cara-

magna Piemonte 44�470N 7�440E, Savigliano 44�390N7�380E, Murello 44�450N 7�360E, Sant’Antonio Baligio

44�330N 7�390E, Racconigi 44�460N 7�410E, Moretta

44�450N 7�320E, Cavallermaggiore 44�430N 7�410E)

(Fig. 1). In the areas considered there are no landfills or

industries of ceramics or paints, being the economy mainly

Fig. 1 Province of Cuneo and

traps location

Bull Environ Contam Toxicol (2014) 93:410–416 411

123

agricultural and pastoral. The municipality of Caramagna

Piemonte is mostly composed of polyphite meadows, with

limited areas used for intensive cultivation. The territory of

the other municipalities considered in this study is used

almost exclusively for intensive cultivation of corn, wheat

and barley.

Crows were euthanized using cervical dislocation, a

method permitted by EU Regulation 1099/2009 (Protection

of Animals at Time of Killing) during a management

program of pest containment. A total of 127 birds were

examined; 84 from Caramagna Piemonte, and the

remaining birds from the other areas. In these areas we

estimated crow density to be 20.3 individuals per km2 (with

95 % CI [16.3–25.3]) using the line-transect method

(Buckland et al 1993) and DISTANCE software. Individ-

uals were examined during the period of August 2005–June

2006. Carcasses were classified by sex and age (Svensson

1992). For age classification, crows were grouped accord-

ing to the following Euring codes: 3 (born in the year in

which they were caught, or young), 5 (born in the year

preceding that in which they were captured, or sub-adult), 6

(born before the year preceding that in which they were

captured, or adults). In order to avoid possible sources of

contamination, liver and kidneys were collected from ani-

mal carcasses by using single-use instruments. Immedi-

ately after sampling, materials were frozen and sent to the

laboratory for analysis.

For digestion, 1 g of liver or kidneys was placed into a

Teflon pressure vessel, and 5 mL of HNO3 (65 %) and

1.5 mL of H2O2 (30 %) were then added. After sealing,

vessels were introduced into a microwave digestion rotor

and the oven was programmed to the following settings:

step 1:8 at 110�C; step 2:2 min at 130�C; step 3:13 min at

200�C. After cooling, digested samples were transferred

into 25 mL measuring tubes. Inner walls of Teflon pressure

vessels were rinsed with ultrapure distilled water and the

rinse water was transferred into the sample-containing

tubes. Ultrapure distilled water, to a final volume of 25 mL,

was then added to the tubes.

Accuracy of analysis was tested using certified reference

material NRCC-DORM-2 Dogfish muscle (National

Research Council of Canada, Ottawa, Canada) Concen-

trations measured in reference material fulfil the range of

the certified values.

Quantitative determination of lead and cadmium was

performed using a Perkin-Elmer AAnalyst 800 Atomic

Absorption Spectrophotometer, equipped with a trans-

versely-heated graphite atomizer (THGA) system, with

Zeeman-effect for background correction and integrated

auto sampler. End cap graphite tubes with a pyrolytic

graphite coating and platforms made of pyrolytic graphite

were used throughout the study. Argon (99.998 % purity)

was used as an inert gas. Cadmium and lead determinations

were carried out by the standard additions method, and the

standard concentrations were 25–50 ng mL-1 for lead and

1–2 ng mL-1 for cadmium. The correlation coefficient

(R) of the calibration curves was 0.99. The detection limit

for Cd was 0.01 and 0.04 mg kg-1 for Pb. All samples

were analyzed in batches and compared with blanks and

samples with known metal content (certified reference

material from the National Bureau of Standards). Recov-

ered concentrations of certified samples were within 10 %

of the certified values. We applied the Shapiro-Wilk test of

normality, the Wilcoxon test for comparing two samples,

the Kruskal-Wallis test for more than two samples and the

Bonferroni procedure for multiple comparisons (Lehmann

and Romano 2005). Thus, we compared the p values with

the conventional level of significance (e.g. 0.05) divided by

the number of simultaneous tests. Statistical analyses were

conducted using R software (version 2.11). Analysis of the

data (and their logarithmic transformation of the data) with

the Shapiro-Wilk test did not allow the use of parametric

tests due to the non-normal distribution of the data itself, so

therefore we adopted a nonparametric approach.

Results and Discussion

Results of metal analysis, calculated in mg kg-1 ww, are

shown in Table 1. We compared lead and cadmium levels

recorded in liver and kidneys from hooded crows, and we

found that lead is stored in a non-significantly different

proportion in the two tissues (W = 7,803, p = 0.987),

while cadmium tends to accumulate more in kidneys than

in the liver (W = 5,206.5, p = 0.000). Lead and cadmium

levels among the three age groups are shown in Table 2,

and results of the statistical analyses are shown in Table 3.

Both in kidneys and liver, the differences of lead and

cadmium levels between the three age categories are highly

significant (p \ 0.001), with the exception of the case of

lead for categories 5 and 6 (in liver: W = 196.5,

p = 0.925; in kidney: W = 174.5, p = 0.0289). Lead and

cadmium levels recorded from category 5 are significantly

higher than those from category 3: for lead in liver

W = 108, p = 0.0003; for lead in kidney W = 610.5,

p = 0.0004; for cadmium in liver W = 463.5, p = 0.0000;

for cadmium in kidney W = 443.5, p = 0.0000. Lead and

cadmium levels recorded from category 6 are significantly

higher than those from category 3: for lead in liver

W = 66.5, p = 0.0009; for lead in kidney W = 190.5,

p = 0.0000; for cadmium in liver W = 82, p = 0.0000;

for cadmium in kidney W = 29, p = 0.0000. Cadmium

levels recorded from category 6 are significantly higher

than those from category 5: in liver W = 120.5,

p = 0.0014; in kidney W = 69.5, p = 0.0000. Moreover,

according to the Bonferroni procedure (Lehmann and

412 Bull Environ Contam Toxicol (2014) 93:410–416

123

Romano 2005), we compared the Wilcoxon p values

reported in Table 3 with the significance level (i.e.,

p \ 0.05) divided by the number of simultaneous tests (i.e.,

3). We also compared levels obtained in the municipality

of Caramagna Piemonte with those of the other munici-

palities considered in this study, and the observed differ-

ences turned out to be highly significant (p \ 0.0001):

median for lead in liver: 0.00 versus 0.08 mg kg-1; median

for cadmium in liver: 0.04 versus 0.19 mg kg-1; median

for lead in kidneys: 0.00 versus 0.11 mg kg-1; median for

cadmium in kidneys: 0.09 versus 0.42 mg kg-1 (as shown

in Table 4). Lead and cadmium levels recorded from males

and females were not found to be significantly different

(Table 5); for lead in liver: W = 481.5, p = 0.904; for

lead in kidneys: W = 472, p = 0.498; for cadmium in

liver: W = 370, p = 0.096; for cadmium in kidneys:

W = 420, p = 0.178. When analysis was limited to age

categories 5 and 6, results still demonstrated no differences

between males and females: for lead in liver: W = 138.5,

p = 0.056; for lead in kidneys: W = 144.5, p = 0.056; for

cadmium in liver: W = 170.5, p = 0.281; for cadmium in

kidneys: W = 144, p = 0.079). Age category 6 alone

(adults): for lead in liver: W = 15, p = 0.079; for lead in

kidneys: W = 23, p = 0.366; for cadmium in liver:

W = 32, p = 1.000; for cadmium in kidneys: W = 30,

p = 0.874).

Hooded crows, when subjected to population control,

could be used as valid bioindicators of environmental

contamination by heavy metals due to their large geo-

graphical distribution, feeding habits and easy sample

collection (Chambers 2008). No heavy metal values

obtained from the liver and kidneys of the target species,

Table 1 Levels of lead and

cadmium in liver and kidneys of

hooded crows in mg kg-1 wet

weight

Organ Metal n Min–max (mg kg-1) Mean (mg kg-1) SD Median (mg kg-1)

Liver Lead 124 0–2.93 0.09 0.27 0.04

Cadmium 124 0–1.75 0.15 0.26 0.06

Kidney Lead 126 0–0.61 0.07 0.10 0.04

Cadmium 126 0.01–9.42 0.39 0.95 0.13

Table 2 Lead and cadmium levels among the three age groups

Organ n Min–max (mg kg-1) Mean (mg kg-1) SD Median (mg kg-1)

Age 3 5 6 3 5 6 3 5 6 3 5 6 3 5 6

Liver Pb 66 30 18 0–0.45 0–0.27 0–2.93 0.06 0.08 0.24 0.10 0.07 0.67 0 0.08* 0.10*

Cd 66 30 18 0–0.25 0.01–0.55 0.02–1.75 0.05 0.16 0.50 0.05 0.17 0.51 0.03 0.09 0.32

Kidney Pb 67 31 18 0–0.40 0–0.27 0–0.61 0.04 0.08 0.17 0.08 0.07 0.14 0 0.08 0.15

Cd 67 31 18 0.01–0.47 0.02–1.02 0.1–9.42 0.11 0.34 1.57 0.01 0.29 2.10 0.08 0.28 1.34

Categories not sharing a common symbol * are significantly different

Table 3 Comparison by age Age code Pb Cd

Liver Kidney Liver Kidney

3 versus 5 versus 6 Kruskal

(v2 = 15.4289;

p = 0.0004463)

Kruskal

(v2 = 27.9929;

p = 8.345e-07)

Kruskal

(v2 = 41.9726;

p = 7.687e-10)

Kruskal

(v2 = 52.5052;

p = 3.969e-12)

3 versus 5 Wilcoxon

(W = 108;

p = 0.0003377)

Wilcoxon

(W = 610.5;

p = 0.0004422)

Wilcoxon

(W= 463.5;

p = 2.744e-05)

Wilcoxon

(W = 443.5;

p = 5.338e-06)

3 versus 6 Wilcoxon

(W = 66.5;

p = 0.000923)

Wilcoxon

(W = 190.5;

p = 1.943e-06)

Wilcoxon

(W = 82;

p = 1.775e-08)

Wilcoxon

(W = 29;

p = 6.353e-10)

5 versus 6 Wilcoxon

(W = 196.5;

p = 0.925)

Wilcoxon

(W = 174.5;

p = 0.02893)

Wilcoxon

(W = 120.5;

p = 0.001443)

Wilcoxon

(W = 69.5;

p = 1.388e-05)

Bull Environ Contam Toxicol (2014) 93:410–416 413

123

comparable with our results, are available from the litera-

ture. Other species of passerines can be considered, but

results for these species concern non-European locations

(Lee et al. 1989; Deng et al. 2007).

The acute lethal dose for lead (LD50), determined by

injection in rats, was found to be 70 mg kg-1 body weight

(Kotsonis and Klaassen 1977), while the dose in wild

passerines is unknown. In Falconiformes, lead content in

the liver and kidneys exceeding 3 mg kg-1 wet weight

(ww) is considered a toxic concentration (Pain et al. 2009).

In Galliformes, levels exceeding 6 mg kg-1 ww in liver

and 15 mg kg-1 in kidneys are considered toxic (Pain et al.

2009). A level as low as 0.16 mg kg-1 in waterfowl can be

toxic (Wachnik 1984). For raptors, a liver content of

7.5 mg kg-1 ww and kidney content of 5 mg kg-1 ww are

suggested as levels of acute lead intoxication with symp-

toms; a liver content that exceeds 1.5 mg kg-1 ww and a

kidney content of 2 mg kg-1 ww is considered a sublethal

level. Lower levels than those mentioned above are con-

sidered deriving from natural exposure to the normal

geochemical background concentrations (Mateo et al.

2003; Kalisinska et al. 2006). Regarding Passeriformes, in

livers of Turdus pallidus, Turdus hortulorum and Turdus

dauma, Lee et al. (1989) was able to detect lead in con-

centrations ranging from 0.81 ± 0.17 mg kg-1 (max

1 mg kg-1) ww. In Chinese Parus major, Deng et al.

(2007) recorded lead concentrations of 1.21 ±

0.37 mg kg-1 dw (dry weight) in kidneys and 0.64 ±

0.15 mg kg-1 dw in liver, while in Carduelis sinica:

0.68 ± 0.08 and 2.59 ± 0.41 mg kg-1 dw of renal lead

and 0.45 ± 0.06 mg kg-1 dw of hepatic lead.

Cadmium in birds is responsible for anorexia, growth

dysfunction, and liver and kidney lesions, as well as having a

negative impact on reproduction and survival. In rats, the

acute lethal dose of cadmium (LD50), administered orally,

was found to be 225 mg kg-1 of body weight. Certain

studies have demonstrated that background cadmium levels

are below 0.9 mg kg-1 ww for freshwater waterfowl (Giulio

and Scanlon 1984; Scheuhammer 1987), whereas concen-

trations greater than 1.5 mg kg-1 ww are considered to be in

excess (Guitart et al. 1994). Regarding the study by Lee et al.

(1989), the amount of cadmium found in Korean Turdus sp.

is 0.81 ± 0.47 (max 1.16) mg kg-1 ww in liver and

2.45 ± 1.37 (max 4.5) mg kg-1 ww in kidneys. In Chinese

P. major, cadmium concentrations were 1.32 ± 0.25 were

dw in kidneys and 0.68 ± 0.1 were dw in liver. In C. sinica,

cadmium levels were 2.59 ± 0.41 were dw in kidneys and

0.56 ± 0.09 were dw in liver (Deng et al. 2007).

In our study, levels of contamination by lead and cad-

mium showed mean values in liver and kidneys that are

consistent with those recorded in C. sinica, P. major, and

Turdus sp. The high tolerance of the hooded crow to heavy

metal, allowed us however to determine exceptional

extreme values of contamination. In particular, we high-

light the value of 9.42 were of cadmium in the kidneys of

an adult male from Murello and to the value of 2.93 were

of lead in the liver of an adult female, also from Murello.

These are extreme values, previously unreported in pas-

serine birds similar to those of carnivorous birds (Hontelez

et al. 1992; Lee et al. 1989; Kalisinska et al. 2006), perhaps

due to their propensity to scavenge.

While lead content is similar in both liver and kidneys,

cadmium tends to accumulate in kidneys, rather than in the

liver, as already observed in other species. The trend to

bioaccumulate in different tissues is evidenced by the sta-

tistically significant differences of the median values,

considering the three age categories: young, sub-adult and

adult. Adults and sub-adults have, on average, higher levels

Table 4 Levels of lead and

cadmium in liver and kidneys

by type of land

M meadows, Int.C. intensive

cultivation

All differences are highly

significant (p \ 0.0001,

Wilcoxon)

Municipality N Min-max (mg/kg) Mean (mg/kg) SD Median (mg/kg)

M Int.C. M Int.C. M Int.C. M Int.C. M Int.C.

Liver Pb 83 41 0–0.45 0–2.93 0.05 0.17 0.09 0.45 0 0.08

Cd 83 41 0–0.51 0.02–1.75 0.06 0.31 0.08 0.39 0.04 0.19

Kidney Pb 83 43 0–0.4 0–0.61 0.05 0.12 0.07 0.12 0 0.11

Cd 83 43 0.01–1.02 0.02–9.42 0.13 0.89 0.15 1.49 0.09 0.42

Table 5 Levels of lead and

cadmium in liver and kidneys

by sex

M males, F females

Organ n Min–max (mg kg-1) Mean (mg kg-1) SD Median (mg kg-1)

M F M F M F M F M F

Liver Pb 35 28 0–0.34 0–2.93 0.07 0.17 0.09 0.55 0.05 0.05

Cd 35 28 0–1.75 0.02–1.33 0.22 0.25 0.38 0.29 0.07 0.11

Kidney Pb 36 29 0–0.33 0–0.61 0.08 0.10 0.10 0.12 0.04 0.07

Cd 36 29 0.01–9.42 0.03–3.13 0.67 0.55 1.59 0.66 0.18 0.28

414 Bull Environ Contam Toxicol (2014) 93:410–416

123

of contamination. Results obtained are in accordance with

previous reports (Kuiters 1996; Falandysz et al. 2005;

Srebocan et al. 2011) for other species. The same trend was

also observed in lead distribution, in contrast with data

reported in other studies (Wolkers et al. 1994; Kuiters

1996) on other species. It is likely that saturation levels of

heavy metals in the involved tissues are reached in the

second year of life.

Male crows, being more dedicated to the pursuit of food,

could be assumed to be more easily exposed to pollution

sources, during the time in which females brood. Our

study, however, suggests that contamination levels are not

affected by sex.

The principal difference between the two habitats

compared in this study is in the practices of agricultural

production: in the municipality of Caramagna Piemonte

there are pastures and meadows dedicated to the production

of hay. The others municipalities are devoted to intensive

cultivation for which inorganic fertilizers are essential to

obtain high productivity. Among the inorganic fertilizers,

phosphorus fertilizers in the Province of Cuneo are still

widely used: 1.6 kg per hectare of area in 2004 (Province

of Cuneo—Settore Agricoltura 2006). However, they

contain heavy metals that can contaminate the soil and

threat the health of animals and humans (Mendes et al.

2006) and European Commission (2014) is aware of the

need to take action in accordance with its risk reduction

strategy. The main source of lead and cadmium contami-

nation, in this study, could be identified as being phosphate

fertilizers. In fact, there is a highly significant difference in

heavy metal contamination between the area dedicated to

meadows and the areas principally devoted to intensive

cultivation. We can consider that the same sources of

contamination may have an important effect on other bird

species whose populations are declining (BTO 2012) and,

in general, on hunted species. The latter could also repre-

sent a risk for public health, if the tissues containing heavy

metals constitute edible parts. Future studies could be

focused on establishing the levels of heavy metals in a

population of hooded crows residing in areas with high

levels of contamination, with particular consideration of

colonies living in urbanized or industrialized areas, in order

to determine tolerance levels and toxicity thresholds of lead

and cadmium for the species.

References

Adams ML, Zhao FJ, McGrath SP, Nicholson FA, Chambers BJ

(2004) Predicting cadmium concentrations in wheat and barley

rain using soil properties. J Environ Qual 33:532–541

Alloway BJ, Steinnes E (1999) Anthropogenic additions of cadmium

to soils. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils

and plants. Kluwer Academic, Dordrecht, pp 97–123

Berglund AMM, Koivula MJ, Eeva T (2011) Species- and age-related

variation in metal exposure and accumulation of two passerine

bird species. Environ Pollut 159(10):2368–2374

Bilandzic N, Sedak M, Ðokic M, Simic B (2010) Wild boar tissue

levels of cadmium, lead and mercury in seven regions of

continental Croatia. Bull Environ Contam Toxicol 84:738–743

BTO (2012) http://www.bto.org/about-birds

Buckland ST, Anderson DR, Burnham KP, Laake JL (1993) Distance

sampling: estimating abundance of biological populations.

Chapman and Hall, London. http://ruwpa.st-and.ac.uk/distance

Burger J (1995) A risk assessment for lead in birds. J Toxicol Environ

Health 45:369–396

Chambers SA (2008) Birds as environmental indicators: review of

literature. Parks Victoria technical series no. 55. Parks Victoria,

Melbourne

Clark AB, Wilson DS (1981) Avian breeding adaptations: hatching

asynchrony, brood reduction, and nest failure. Q Rev Biol

56:253–277

Council Regulation (EC) No 1099/2009 of 24 September 2009 on the

protection of animals at time of killing. Off J Eur Union L303/1.

18 Nov 2009

Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M (2000) Can

excrement and feathers of nestling songbirds be used as

biomonitors for heavy metal pollution? Arch Environ Contam

Toxicol 39:541–546

Deng H, Zhang Z, Chang C, Wang Y (2007) Trace metal concen-

tration in Great Tit (Parus major) and Greenfinch (Carduelis

sinica) at the Western Mountains of Beijing, China. Environ

Pollut 148:620–626

European Commission (2014) Commission recommendation of 4

April on the reduction of the presence of cadmium in foodstuffs

Falandysz J, Szymczyk-Kobrzynska K, Brzostowski A, Zalewski K,

Zasadowski A (2005) Concentration of heavy metals in the tissue

of red deer (Cervus elaphus) from the region of Warmia and

Mazury, Poland. Food Addit Contam 22:141–149

Gainer JH (1974) Lead aggravates viral disease and represses the

antiviral activity of interferon inducers. Environ Health Perspect

7:113–119

Giulio RT, Scanlon PF (1984) Heavy metals in tissues of waterfowl

from the Chesapeake Bay, USA. Environ Pollut 35:29–48

Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P,

Reich A, Groneberg DA (2006) The toxicity of cadmium and

resulting hazards for human health. J Occup Med Toxicol

1:22–28

Guitart R, To-Figueras J, Mateo R, Bertolero A, Cerradelo S,

Martınez-Vilalta A (1994) Lead poisoning in waterfowl from the

Ebro Delta, Spain: calculation of lead exposure thresholds for

mallards. Arch Environ Contam Toxicol 27:289–293

Hontelez LCMP, van den Dungen HM, Baars JA (1992) Lead and

cadmium in birds in The Netherlands: a preliminary survey.

Arch Environ Contam Toxicol 23:453–456

Kalisinska E, Salicki W, Jackowski A (2006) Six trace metals in

white-tailed eagle from Northwestern Poland. Pol J Environ Stud

15:727–737

Kotsonis FN, Klaassen CD (1977) Toxicity and distribution of

cadmium administered to rats at sublethal doses. Toxicol Appl

Pharmacol 41:667–680

Krajnc EI, van Gestel CAM, Mulder HCM, de Vrijer FI, Sinkeldam

EJ, Vink GJ, Canton JH, van Apeldoom ME, Janus JA (1987)

Integrated criteria document. Cadmium—effects. Appendix.

Bilthoven, National Institute of Public Health and Environmental

Protection (Report No. 758476004)

Kuiters AT (1996) Accumulation of cadmium and lead in red deer

and wild boar at the Velewue, the Netherlands. Vet Q

18:134–135

Bull Environ Contam Toxicol (2014) 93:410–416 415

123

Lee DP, Honda K, Tatsukawa R, Won PO (1989) Distribution and

residue level of mercury, cadmium and lead in Korean birds.

Bull Environ Contam Toxicol 43:550–555

Lehmann EL, Romano JP (2005) Testing statistical hypotheses.

Springer, New York

Markowski M, Banbura M, Kalinski A, Markowski J, Skwarska J,

Zielinski P, Wawrzyniak J, Ban J (2013) Avian feathers as

biondicators of the exposure to heavy metal contamination of

food. Bull Environ Contam Toxicol 91:302–305

Mateo R, Taggart M, Meharg AA (2003) Lead and arsenic in bones of

birds of prey from Spain. Environ Pollut 126:107

Mendes AMS, Duda GP, Araujo do Nascimento CW, Silva MO

(2006) Bioavailability of cadmium and lead in a soil amended

with phosphorus fertilizers. Sci Agric (Piracicaba, Braz) 63,

4:328–332

Mora MA (2013) Heavy metals and metalloids in egg contents and

eggshells of passerine birds from Arizona. Environ Pollut

125:393–400

Pain DJ, Fisher IJ, Thomas VG (2009) A global update of lead

poisoning in terrestrial birds from ammunition sources. In:

Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of

spent lead ammunition: implications for wildlife and humans.

The Peregrine Fund, Boise

Province of Cuneo (2006) Prima relazione sullo stato dell’ambiente:

http://www.provincia.cuneo.gov.it/allegati/node/954/primare

lazionesullostatodell’ambientedellapr19752.pdf

Scheuhammer AM (1987) The chronic toxicity of aluminum,

cadmium, mercury, and lead in birds: a review. Environ Pollut

46:263–295

Sheppard SC, Grant CA, Sheppard MI, De Jong R, Long J (2009)

Risk indicator for agricultural inputs of trace elements to

Canadian soils. J Environ Qual 38:919–932

Spellerberg IF (1991) Monitoring ecological change. Cambridge

University Press, Cambridge

Srebocan E, Crnic AP, Ekert-Kabalin AM, Lazarus M, Jurasovic J,

Tomljanovic K, Andreic D, Perovic IS, Coz-Rakovac R (2011)

Cadmium, lead, and mercury concentrations in tissues of roe

deer (Capreolus capreolus L.) and wild boar (Sus scrofa L.) from

lowland Croatia. Czechoslov J Food Sci 29:624–633

Svensson L (1992) Identification guide to European passerines, 4th

edn. Stockholm, Sweden

Swaileh KM, Sansur R (2006) Monitoring urban heavy metal

pollution using the House Sparrow (Passer domesticus). J Envi-

ron Monit 8:209–213

Wachnik Z (1984) Poultry diseases. PWN, Warszawa

Wolkers H, Wensing T, Geert WTA, Bruinderink G (1994) Heavy

metal contamination in organs in red deer (Cervus elaphus) and

wild boar (Sus scrofa) and the effect on some trace elements. Sci

Total Environ 144:191–199

416 Bull Environ Contam Toxicol (2014) 93:410–416

123